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. 1984 Aug;81(16):5165–5169. doi: 10.1073/pnas.81.16.5165

Different evolutionary behavior of structurally related, repetitive sequences occurring in the same Balbiani ring gene in Chironomus tentans

Christer Höög 1, Lars Wieslander 1,*
PMCID: PMC391658  PMID: 16593501

Abstract

The Balbiani ring 2 (BR 2) gene in Chironomus tentans is highly internally repeated. Two types of related repeat units—the α and β types—are tandemly arranged in separate blocks, which together are likely to form the major part of the gene. Every repeat unit has one constant region and one subrepeat region. Here we analyze the length and sequence of a number of repeat units of both types and compare the units within and between the blocks. The ≈100 α repeat units are essentially invariant regarding length and sequence. In contrast, when the ≈70 β repeat units are compared, six length variants are found, four of which have been sequenced. The length variations reside in the subrepeat regions and are due to different numbers of whole or half subrepeats. Furthermore, the subrepeat regions differ by several base-pair substitutions, many of which change the amino acid sequence. On the other hand, all β-type constant regions are of equal length and are virtually homogeneous in sequence. The observed length distributions in combination with analysis of the basepair substitutions in the α-and β-type constant and subrepeat regions suggest that the α and β blocks are of different age, that seemingly homologous repeated regions may play different functional roles at the protein level, and that sequence correction mechanisms are likely to operate to different extents on the constant and subrepeat regions within the β block.

Keywords: molecular evolution, gene structure, structural proteins, gene family

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Selected References

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  1. Baltimore D. Gene conversion: some implications for immunoglobulin genes. Cell. 1981 Jun;24(3):592–594. doi: 10.1016/0092-8674(81)90082-9. [DOI] [PubMed] [Google Scholar]
  2. Bäumlein H., Wobus U., Gerbi S. A., Kafatos F. C. The basic repeat unit of a Chironomus Balbiani ring gene. Nucleic Acids Res. 1982 Jul 10;10(13):3893–3904. doi: 10.1093/nar/10.13.3893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bäumlein H., Wobus U., Gerbi S., Kafatos F. C. Characterization of a 249-bp tandemly repetitive, satellite-like repeat in the translated portion of Balbiani ring c of Chironomus thummi. EMBO J. 1982;1(5):641–647. doi: 10.1002/j.1460-2075.1982.tb01221.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Case S. T., Byers M. R. Repeated nucleotide sequence arrays in Balbiani ring 1 of Chironomus tentans contain internally nonrepeating and subrepeating elements. J Biol Chem. 1983 Jun 25;258(12):7793–7799. [PubMed] [Google Scholar]
  5. Case S. T., Summers R. L., Jones A. G. A variant tandemly repeated nucleotide sequence in Balbiani ring 2 of Chironomus tentans. Cell. 1983 Jun;33(2):555–562. doi: 10.1016/0092-8674(83)90436-1. [DOI] [PubMed] [Google Scholar]
  6. Eiferman F. A., Young P. R., Scott R. W., Tilghman S. M. Intragenic amplification and divergence in the mouse alpha-fetoprotein gene. Nature. 1981 Dec 24;294(5843):713–718. doi: 10.1038/294713a0. [DOI] [PubMed] [Google Scholar]
  7. Jäckle H., Almeida J. C., Galler R., Kluding H., Lehrach H., Edström J. E. Constant and variable parts in the Balbiani ring 2 repeat unit and the translation termination region. EMBO J. 1982;1(7):883–888. doi: 10.1002/j.1460-2075.1982.tb01264.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Lamb M. M., Daneholt B. Characterization of active transcription units in Balbiani rings of Chironomus tentans. Cell. 1979 Aug;17(4):835–848. doi: 10.1016/0092-8674(79)90324-6. [DOI] [PubMed] [Google Scholar]
  9. Muskavitch M. A., Hogness D. S. An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell. 1982 Jul;29(3):1041–1051. doi: 10.1016/0092-8674(82)90467-6. [DOI] [PubMed] [Google Scholar]
  10. Ohno S., Epplen J. T. The primitive code and repeats of base oligomers as the primordial protein-encoding sequence. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3391–3395. doi: 10.1073/pnas.80.11.3391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ohno S., Kato K., Hozumi T., Matsunaga T. Mouse immunoglobulin coding sequences for the heavy-chain variable region arose as repeats of the two short building blocks. Proc Natl Acad Sci U S A. 1982 Jan;79(1):132–136. doi: 10.1073/pnas.79.1.132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ohno S., Matsunaga T., Epplen J. T., Itakura K., Wallace R. B. Identification of the 45-base-long primordial building block of the entire class I major histocompatibility complex antigen gene. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6342–6346. doi: 10.1073/pnas.79.20.6342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ohno S. Original domain for the serum albumin family arose from repeated sequences. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7657–7661. doi: 10.1073/pnas.78.12.7657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pech M., Streeck R. E., Zachau H. G. Patchwork structure of a bovine satellite DNA. Cell. 1979 Nov;18(3):883–893. doi: 10.1016/0092-8674(79)90140-5. [DOI] [PubMed] [Google Scholar]
  15. Rydlander L., Edström J. E. Large sized nascent protein as dominating component during protein synthesis in Chironomus salivary glands. Chromosoma. 1980;81(1):85–99. doi: 10.1007/BF00292424. [DOI] [PubMed] [Google Scholar]
  16. Sanger F., Coulson A. R. The use of thin acrylamide gels for DNA sequencing. FEBS Lett. 1978 Mar 1;87(1):107–110. doi: 10.1016/0014-5793(78)80145-8. [DOI] [PubMed] [Google Scholar]
  17. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]
  19. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  20. Sprague K. U., Roth M. B., Manning R. F., Gage L. P. Alleles of the fibroin gene coding for proteins of different lengths. Cell. 1979 Jun;17(2):407–413. doi: 10.1016/0092-8674(79)90167-3. [DOI] [PubMed] [Google Scholar]
  21. Sun Y. L., Xu Y. Z., Chambon P. A simple and efficient method for the separation and detection of small DNA fragments by electrophoresis in formamide containing agarose gels and Southern blotting to DBM-paper. Nucleic Acids Res. 1982 Oct 11;10(19):5753–5763. doi: 10.1093/nar/10.19.5753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sümegi J., Wieslander L., Daneholt B. A hierarchic arrangement of the repetitive sequences in the Balbiani ring 2 gene of Chironomus tentans. Cell. 1982 Sep;30(2):579–587. doi: 10.1016/0092-8674(82)90254-9. [DOI] [PubMed] [Google Scholar]
  23. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tsujimoto Y., Suzuki Y. The DNA sequence of Bombyx mori fibroin gene including the 5' flanking, mRNA coding, entire intervening and fibroin protein coding regions. Cell. 1979 Oct;18(2):591–600. doi: 10.1016/0092-8674(79)90075-8. [DOI] [PubMed] [Google Scholar]
  25. Wieslander L., Lendahl U. The Balbiani ring 2 gene in Chironomus tentans is built from two types of tandemly arranged major repeat units with a common evolutionary origin. EMBO J. 1983;2(7):1169–1175. doi: 10.1002/j.1460-2075.1983.tb01563.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wieslander L., Sümegi J., Daneholt B. Evidence for a common ancestor sequence for the Balbiani ring 1 and Balbiani ring 2 genes in Chironomus tentans. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6956–6960. doi: 10.1073/pnas.79.22.6956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yamada Y., Avvedimento V. E., Mudryj M., Ohkubo H., Vogeli G., Irani M., Pastan I., de Crombrugghe B. The collagen gene: evidence for its evolutinary assembly by amplification of a DNA segment containing an exon of 54 bp. Cell. 1980 Dec;22(3):887–892. doi: 10.1016/0092-8674(80)90565-6. [DOI] [PubMed] [Google Scholar]

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